Estrogen activation of the mitogen-activated protein kinase is mediated by ER-α36 in ER-positive breast cancer cells

J Steroid Biochem Mol Biol. 2014 Sep:143:434-43. doi: 10.1016/j.jsbmb.2014.06.009. Epub 2014 Jun 25.

Abstract

It is well known that there are two estrogen-signaling pathways, genomic estrogen signaling and non-genomic or rapid estrogen signaling. Although both ER-α and ER-β have been suggested to mediate both genomic and non-genomic estrogen signaling, rapid estrogen signaling such as activation of the MAPK/ERK signaling in ER-positive breast cancer MCF7 cells has been controversial. Previously, our laboratory cloned a 36kDa variant of ER-α, ER-α36, that is mainly localized at the plasma membrane and is able to mediate rapid estrogen signaling. In this study, we investigated the function and the underlying mechanisms of ER-α36 in rapid estrogen signaling of ER-positive breast cancer cells. ER-positive breast cancer cells MCF7, T47D and H3396 as well as their variants with different levels of ER-α and ER-α36 expression were used to examine estrogen induction of the MAPK/ERK1/2 signaling. The underlying mechanisms were also studied in these cells with the neutralizing antibodies and chemical inhibitors against different growth factors and their receptors. We found that ER-α36 mediated estrogen induction of the MAPK/ERK phosphorylation in ER-positive breast cancer cells while the full-length ER-α failed to do so. The rapid estrogen signaling mediated by ER-α36 involved a orchestrated action of matrix metalloproteinases (MMPs), heparin-binding epidermal growth factor (HB-EGF), amphiregulin, insulin-like growth factor 1 receptor (IGF-1R), epidermal growth factor receptor (EGFR), HER2/Neu and Src. Our results thus indicated that ER-α36 is the estrogen receptor that mediates estrogen induction of the MAPK/ERK signaling in ER-positive breast cancer cells.

Keywords: Amphiregulin; EGFR; ER-α36; ERK1/2; HB-EGF; HER2; IGF-IR; Rapid estrogen signaling.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Apoptosis / drug effects
  • Blotting, Western
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Cell Cycle / drug effects
  • Cell Proliferation / drug effects
  • Estrogen Receptor alpha / genetics
  • Estrogen Receptor alpha / metabolism*
  • Estrogens / pharmacology*
  • Female
  • Flow Cytometry
  • Humans
  • Mitogen-Activated Protein Kinases / metabolism*
  • Phosphorylation / drug effects
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptor, ErbB-2 / genetics
  • Receptor, ErbB-2 / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • Tumor Cells, Cultured

Substances

  • ESR1 protein, human
  • Estrogen Receptor alpha
  • Estrogens
  • RNA, Messenger
  • Receptor, ErbB-2
  • Mitogen-Activated Protein Kinases